Though intensive agriculture ensures food security worldwide, it affects soil health, water availability, human health, animal health, and environmental health (Jian et al. 2020; Lehmann et al. 2020). Apart from this, the crop's resilience to biotic and abiotic stresses under intensive agro-systems is low, as the cultivars and hybrids developed for the present agricultural systems have neglected the plant-associated microbiome. The root-associated microbiome and its functioning are considered significant factors affecting crop growth, yield, and resistance against biotic and abiotic stresses under sustainable agriculture (Nerva et al. 2022). The landraces recruit their rhizo-microbiome depending on the soil and environmental factors, while the high-yielding cultivars fail to form a potential host-microbiome interaction, hence unsuccessful in performing when unexpected drought, pest, and diseases occur (Chang et al. 2022). Therefore, understanding the mechanisms of microbiome interaction by landraces will help to develop interventions for the growth and fitness of high-yielding cultivars to ensure sustainability. Though several reports on the impact of cultivars and moisture-stress conditions on rice rhizosphere are available, no comprehensive report on both soil biochemical attributes and rhizo-microbiome analyses was documented yet. The present study provides vital information on rhizosphere functioning and rhizosphere-associated microbial communities of two contrasting genotypes of rice grown under the same soil conditions after a 25-days long drought. Though most of the biological attributes of rhizosphere soil got affected due to drought, the landrace Norungan assimilated resilience and accounted for less impact than the high-yielding cultivar, Co51. Likewise, the rhizosphere microbiome shift also varied between Norungan and Co51 when the crops were exposed to drought. We also identified the differential microbial taxa of each genotype that may possess specific ecological functioning in their host plants.
The comprehensive results of the present work on rhizosphere's biochemical attributes revealed that most of the assessed variables, including soil organic carbon, biomass carbon, labile carbon, and enzymes like dehydrogenase, urease, and phosphatase, were significantly higher in Norungan rhizosphere than in the Co51 rhizosphere. When the drought was introduced, all these assessed attributes decreased considerably in both genotypes' rhizosphere. However, resilience in carbon pools and biochemical attributes was observed in the Norungan rhizosphere but not in the Co51.
The soil carbon pool is composed of soil organic and inorganic carbon, which plays a vital role in the carbon cycle. Soil organic carbon equilibrium is governed by several interacting factors such as temperature, moisture, texture, quantity, and quality of organic matter, methods of organic matter application, soil tillage, cultivation methods, and cropping system (Vineela et al. 2008). In the present investigation, the rhizosphere's organic carbon had a significant impact due to genotypes and moisture stress, and Norungan > Co51 and normal > drought were the trend observed. Microbial biomass carbon, the measure of the living component of soil organic carbon, is the potential indicator representing soil's microbial activity and nutrient dynamics (Anderson and Domsch 1985). In the present work, the landrace Norungan had significantly higher biomass in the rhizosphere than Co51, indicating that the Norungan rhizosphere harbors more microbiome than Co51. The drought affected the soil MBC, irrespective of crop genotype and niche. This implies the detrimental impacts of drought on soil microbial activities. The labile carbon represents the readily available carbon to be utilized by the soil microorganisms. An increased soil labile carbon level indicates high microbial proliferation, soil health, and fertility (Ramírez et al. 2020). As the root exudates comprise a high proportion of readily available carbon substrates, the labile soil carbon would always be higher in the rhizosphere than bulk soil, irrespective of crop or genotype (Bhattacharyya et al. 2019). In the present work, the Norungan rhizosphere accounted for nearly 30% higher SLC than Co51, indicating that the landrace Norungan releases much higher levels of exudation than Co51, which was used as a trap to attract soil-borne microorganisms and thereby formed diversified and functionally active microbiome than Co51. The substrate-induced respiration and metabolic quotient of rhizosphere soils of Co51 and Norungan were compared with bulk soils and moisture stress conditions. These two respiration indices are potential sensitive indicators of soil microbial activity and are used to monitor soil microbial metabolism (Anandakumar et al. 2022; Tamilselvi et al. 2015). The substrate-induced respiration rate is high when the soil's microbial population is active. When the microbes receive adequate resources, the metabolic quotient (basal respiration) is low. In other words, a low metabolic quotient indicates the minimal energy required to maintain microbial function (Anderson and Lebepe-Mazur 2003). In the present work, the rhizosphere soils of Co51 and Norungan accounted for higher substrate-induced respiration and lower metabolic quotient than bulk soils. The difference between Norungan and Co51 in terms of respiration indices is trivial. However, when drought was induced, the Norungan had a higher response in respiration rates than Co51, indicating that the drought-responsive rhizosphere functioning is higher for landraces than cultivars. Soil enzymes, viz., dehydrogenase, urease, and phosphatase, are sensitive indicators of soil health, and the rhizosphere always accounted for higher activities than bulk soils (Xu et al. 2022). In the present investigation, the landrace Norungan rhizosphere accounted for significantly higher enzyme activities than Co51, and drought had a significantly deleterious impact on these enzymes for Co51 but less for Norungan. These results are in accordance with the other biological attributes reported in this study.
Rhizosphere functioning is essential for every plant as it regulates its nutrients and water flow. The natural plant recruits its microbiome in the rhizosphere to do these functions through a synchronized approach. However, when high-yielding cultivars are developed through breeding programs, we omitted these rhizosphere-mediated traits; hence, the rhizosphere functioning may not be as expected. Under that circumstances, the crop heavily depends on synthetic chemical fertilizers for readily available nutrients. Further, the plant cannot withstand the biotic and abiotic stresses due to the less-functional rhizosphere (Abdullaeva et al. 2021; Chang et al. 2022; Nerva et al. 2022; Ray et al. 2020; Sun et al. 2021b). In the present work, we showed that the drought-tolerant landrace Norungan and high-yielding cultivar Co51 performed more or less similar rhizosphere functioning under normal conditions. Still, when drought was enforced, the Norungan rhizosphere showed resilience and maintained its rhizosphere functioning as that of normal moisture condition. The high-yielding cultivar Co51 exhibited less rhizosphere functioning under drought conditions. The possible reasons for the drought-affected rhizosphere functioning are (1) drought-induced osmotic stress causing cell lysis and microbial death, significantly reducing the microbial biomass and its functioning (Turner et al. 2003). In addition, the root exudation of the host plant affected both qualitatively and quantitatively and led to the loss of nutrient resources for the microbiome (Williams et al. 2020). The consequences of these two effects were noticed in the present work. The microbial biomass and related variables, viz., respiration and enzymes, got reduced in drought-induced soil compared with normal moisture soil, irrespective of rhizosphere and bulk soil. Further, the functioning of the Norungan rhizosphere got plasticity in drought-induced conditions but not in the Co51 rhizosphere. Norungan grew without reducing the plant biomass and root system when the drought was introduced. Hence the rhizosphere functioning was less affected. In contrast, Co51 got affected by its root system by drought, which explained the reason for significantly reduced biological attributes. Similar consequences were reported in the rhizospheres of different grass species (Bouasria et al. 2012; de Vries et al. 2019; Sanaullah et al. 2011; Wang et al. 2021; Xiao et al. 2022; Xue et al. 2017) and maize (Zhang et al. 2021a; Zhang et al. 2021b) at drought-induced conditions.
Rice harbor diversified microflora in the rhizosphere, rhizoplane, phyllosphere, and endosphere, which includes nitrogen fixers, nitrifiers, plant growth regulators, methanogens, methane oxidizers, sulfur oxidizers, mineral solubilizers, and decomposers (Kumar et al. 2017; Prasanna et al. 2012). The soil's physico-chemical properties, climatic factors, and cultivation methods play a significant role in shaping the rice microbiome (Kim et al. 2020; Xu et al. 2020). The genotypes also play a crucial role in shaping the rice microbiome (Edwards et al. 2015). The predominant phyla reported across different rice cultivars [six cultivars, viz., Nipponebare, IR50, M109, 93-11, TOg7102, and TOg7267] are Acidobacteria, Actinobacteria, Bacteroides, Chloroflexi, Firmicutes, Gemmatimonadetes, Nitrospirae, Planctomycetes, Proteobacteria, and Verrucomicrobia (Edwards et al. 2015). The japonica rice cultivar Koral also accounted for the same groups of phyla (Hernández et al. 2015). Xiong et al. (2021) identified the common and differentially abundant rhizosphere microbiome of two cultivars and one hybrid rice. In the present work, we documented Acidobacteria, Actinobacteria, Chloroflexi, Firmicutes, Gemmatimonadetes, Nitrospirae, Proteobacteria, Rokubacteria, and Verrucomicrobia as predominant phyla in Norungan and Co51 rice rhizospheres. The results revealed that the bulk soils and rhizosphere soils shared a common microbiome but varied in abundance. This implies the recruitment of the rhizosphere microbiome from bulk soils, and we have not found any specific phyla to the rhizosphere alone. The Norungan rhizosphere accounted for a decreased proportion of proteobacteria and an increased proportion of Firmicutes due to drought, while in the Co51 rhizosphere, this change of phyla is insignificant.
Microbe-mediated drought mitigation of crops through rhizosphere harnessing is a complementary approach to reducing crop loss due to drought (de Vries et al. 2020). When the drought is enforced on a crop, compartment-specific reconstruction of microbiota occurs in rice (Santos-Medellín et al. 2017). A predominant increase of Actinobacteria, Chloroflexi, and Firmicutes due to drought was reported in rice across different genotypes (Santos-Medellín et al. 2017; Santos-Medellín et al. 2021; Zhang et al. 2018). In the present work, we observed that the Norungan rhizosphere drastically reduced its Firmicutes due to drought, while the Co51 rhizosphere remained unchanged. In contrast, the Proteobacteria got enhanced abundance due to drought in Norungan, while the Co51 accounted for the reduced abundance of Proteobacteria. We also reported that the rhizosphere microbiome of rice remained the same when the genotypes were grown under normal conditions. Still, when drought-induced, the landrace and cultivar responded differentially in accommodating their root microbiome, especially the recruitment of Proteobacteria, Actinobacteria, Firmicutes, and Acidobacteria. Among the two genotypes, the landrace Norungan showed significant resilience in its rhizosphere functioning, assuming that the microbiome recruitment during drought is more prominent than in the high-yielding cultivar. High-level of conservation and microbiome shift by Norungan suggest that the recruitment strategy of landraces, wild species, and native plants in rhizosphere microbiome assemblage is better than high-yielding cultivars and hybrids (Santos-Medellín et al. 2021).
Our study affords a comprehensive description of the effect of drought stress on rhizosphere functioning and root-associated microbiomes of two contrasting rice genotypes. Our results revealed that the rice landrace Norungan mitigates the drought through its microbiome recruitment, thereby maintaining its rhizosphere and growth as normal moisture conditions. Hence, it is suggested from our study that the rhizosphere functioning and rhizo-microbiome analyses may be included as essential traits in breeding programs for developing drought-tolerant rice varieties. In addition, the drought-responsive microorganisms with plant-growth promotion and drought mitigation from Norungan can be explored for developing synthetic microbial community inoculants as a mimic to the natural rhizosphere microflora for sustainable rice production.